Mechanical properties of bone tissues with greatly differing functions

Currey, J. D.

Affiliations

¹Department of Biology, University of York, York, Y01 5DD, England

Abstract

The mechanical properties of three types of bone: deer's antler, cow's femur and fin whale's tympanic bulla, are compared. The antler has a very high work of fracture, the bulla a very low one. The bulla has a very high modulus of elasticity, the antler a low one. The cow's femur is the strongest in bending, the bulla is very weak. It is shown how these mechanical properties, which are associated with markedly different amounts of mineralization, nicely suit the bones for their differeing functions.

Links

DOI: 10.1016/0021-9290(79)90073-3

PubMed: 468855

WoS: A1979GV42500008

History

Received: 1978-08-25

Cited Works (9)

Year	Entry
1959	Vose GP, Kubala AL Jr. Bone strength: its relationship to x-ray determined ash content. Hum Biol. September 1959;31:261-270.
1965	Sedlin ED. A rheologic model for cortical bone: a study of physical properties of human femoral samples. Acta Orthop Scand. 1965;(suppl 83):1-77.
1976	Carter DR, Hayes WC, Schurman DJ. Fatigue life of compact bone, II: effects of microstructure and density. J Biomech. 1976;9(4):211-218.
1968	Currey JD. The effect of protection on the impact strength of rabbits’ bones. Acta Anat. 1968;71(1):87-93.
1966	Tattersall HG, Tappin G. The work of fracture and its measurement in metals, ceramics and other materials. J Mater Sci. 1966;1(3):296-301.
1976	Wainwright SA, Biggs WD, Currey JD, Gosline JM. Mechanical Design in Organisms. London, UK: Edward Arnold; 1976.
1969	Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech. March 1969;2(1):1-11.
1975	Currey JD, Butler G. The mechanical properties of bone tissue in children. J Bone Joint Surg. September 1975;57A(6):810-814.
1975	Currey JD. The effects of strain rate, reconstruction and mineral content on some mechanical properties of bovine bone. J Biomech. 1975;8(1):81-86.

Cited By (63)

Year	Entry
1984	Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc Lond B Biol Sci. February 13, 1984;304(1121):509-518.
2002	Currey JD. Bones: Structure and Mechanics. Princeton, NJ: Princeton University Press; 2002.
2008	Akhtar R, Daymond MR, Almer JD, Mummery PM. Elastic strains in antler trabecular bone determined by synchrotron x-ray diffraction. Acta Biomater. 2008;4(6):1677-1687.
2009	Chen P-Y, Stokes AG, McKittrick J. Comparison of the structure and mechanical properties of bovine femur bone and antler of the North American elk (Cervus elaphus canadensis). Acta Biomater. February 2009;5(2):693-706.
2010	Launey ME, Chen P-Y, McKittrick J, Ritchie RO. Mechanistic aspects of the fracture toughness of elk antler bone. Acta Biomater. April 2010;6(4):1505-1514.
2004	Wang X, Puram S. The toughness of cortical bone and its relationship with age. Ann Biomed Eng. January 2004;32(1):123-135.
2010	Launey ME, Buehler MJ, Ritchie RO. On the mechanistic origins of toughness in bone. Ann Rev Mater Sci. 2010;40:25-53.
1997	Bloebaum RD, Skedros JG, Vajda EG, Bachus KN, Constantz BR. Determining mineral content variations in bone using backscattered electron imaging. Bone. May 1997;20(5):485-490.
2008	Ritchie RO, Koester KJ, Ionova S, Yao W, Lane NE, Ager JW III. Measurement of the toughness of bone: a tutorial with special reference to small animal studies. Bone. November 2008;43(5):798-812.
2020	Razi H, Predan J, Fischer FD, Kolednik O, Fratzl P. Damage tolerance of lamellar bone. Bone. January 2020;130:115102.
2020	Willie BM, Zimmermann EA, Vitienes I, Main RP, Komarova SV. Bone adaptation: safety factors and load predictability in shaping skeletal form. Bone. February 2020;131:115114.
1982	Leichter I, Margulies JY, Weinreb A, Mizrahi J, Robin GC, Conforty B, Makin M, Bloch B. The relationship between bone density, mineral content, and mechanical strength in the femoral neck. Clin Orthop Relat Res. March 1982;163:272-281.
1989	Weiner S, Traub W. Crystal size and organization in bone. Connect Tissue Res. 1989;21(1-4):259-265.
2000	Zioupos P, Currey JD, Casinos A. Exploring the effects of hypermineralisation in bone tissue by using an extreme biological example. Connect Tissue Res. 2000;41(3):229-248.
2003	Judex S, Boyd S, Qin Y-X, Miller L, Müller R, Rubin C. Combining high-resolution micro-computed tomography with material composition to define the quality of bone tissue. Curr Osteoporos Rep. June 2003;1(1):11-19.
1984	Lipson SF, Katz JL. The relationship between elastic properties and microstructure of bovine cortical bone. J Biomech. 1984;17(4):231-240.
1990	Jaslow CR. Mechanical properties of cranial sutures. J Biomech. 1990;23(4):313-321.
1997	Vashishth D, Behiri JC, Bonfield W. Crack growth resistance in cortical bone: concept of microcrack toughening. J Biomech. August 1997;30(8):763-769.
2003	Vashishth D, Tanner KE, Bonfield W. Experimental validation of a microcracking-based toughening mechanism for cortical bone. J Biomech. January 2003;36(1):121-124.
2003	Currey JD. The many adaptations of bone. J Biomech. 2003;36(10):1487-1495.
2004	Currey JD. Tensile yield in compact bone is determined by strain, post-yield behaviour by mineral content. J Biomech. April 2004;37(4):549-556.
2005	Tommasini SM, Nasser P, Schaffler MB, Jepsen KJ. Relationship between bone morphology and bone quality in male tibias: implications for stress fracture risk. J Bone Miner Res. August 2005;20(8):1372-1380.
2015	Jepsen KJ, Silva MJ, Vashishth D, Guo XE, van der Meulen MCH. Establishing biomechanical mechanisms in mouse models: practical guidelines for systematically evaluating phenotypic changes in the diaphyses of long bones. J Bone Miner Res. June 2015;30(6):951-966.
1982	Rubin CT, Lanyon LE. Limb mechanics as a function of speed and gait: a study of functional strains in the radius and tibia of horse and dog. J Exp Biol. December 1982;101:187-211.
1999	Currey JD. What determines the bending strength of compact bone? J Exp Biol. September 1999;202(18):2495-2503.
1999	Currey JD. The design of mineralised hard tissues for their mechanical functions. J Exp Biol. December 1999;202(23):3285-3294.
2009	Currey JD, Landete-Castillejos T, Estevez J, Ceacero F, Olguin A, Garcia A, Gallego L. The mechanical properties of red deer antler bone when used in fighting. J Exp Biol. 2009;212(24):3985-3993.
2010	Currey JD. Mechanical properties and adaptations of some less familiar bony tissues. J Mech Behav Biomed Mater. July 2010;3(5):357-372.
2011	Chen P-Y, McKittrick J. Compressive mechanical properties of demineralized and deproteinized cancellous bone. J Mech Behav Biomed Mater. October 2011;4(7):961-973.
2002	Les CM, Stover SM, Keyak JH, Taylor KT, Kaneps AJ. Stiff and strong compressive properties are associated with brittle post‐yield behavior in equine compact bone material. J Orthop Res. May 2002;20(2):607-614.
2004	Currey J. Incompatible mechanical properties in compact bone. J Theo Biol. December 21, 2004;231(4):569-580.
1989	Currey JD, Pond CM. Mechanical properties of very young bone in the axis deer (Axis axis) and humans. J Zool. May 1989;218(1):59-67.
1997	Zioupos P, Currey JD, Casinos A, De Buffrénil V. Mechanical properties of the rostrum of the whale Mesoplodon densirostris, a remarkably dense bony tissue. J Zool. 1997;241(4):725-737.
1998	Zioupos P. Recent developments in the study of failure of solid biomaterials and bone: “fracture” and “pre-fracture” toughness. Mater Sci Eng C Mater Biol Appl. September 1998;6(1):33-40.
1994	Zioupos P, Currey JD, Sedman AJ. An examination of the micromechanics of failure of bone and antler by acoustic emission tests and laser scanning confocal microscopy. Med Eng Phys. May 1994;16(3):203-212.
2011	Bonney H, Colston BJ, Goodman AM. Regional variation in the mechanical properties of cortical bone from the porcine femur. Med Eng Phys. May 2011;33(4):513-520.
2007	Taylor D, Hazenberg JG, Lee TC. Living with cracks: damage and repair in human bone. Nat Mater. April 2007;6(4):263-268.
2001	Currey JD, Zioupos P, Peter D, Casinos A. Mechanical properties of nacre and highly mineralized bone. Proc R Soc B. January 7, 2001;268(1462):107-111.
1996	Hillam RA. Response of Bone to Mechanical Load and Alterations in Circulating Hormones [PhD thesis]. Bristol, UK: University of Bristol; October 1996.
2018	Seek TW. Exploration of Unique Porous Bone Materials for Candidacy in Bioinspired Material Design [Master's thesis]. Colorado State University; Spring 2018.
2008	Tommasini SM. Phenotypic Integration Contributes to Skeletal Functionality and Fragility [PhD thesis]. New York, NY: The City University of New York; 2008.
2007	Akhtar R. Micromechanical Behaviour of Bone [PhD thesis]. University of Manchester; 2007.
2011	Storvik SG. Development of an Experimental Model to Quantify Lumbar Spine Kinematics During Military Seat Ejection [Master's thesis]. Marquette University; August 2011.
2008	Booker WA. Forgiveness of Genetic Variation: Functional Interactions Among Bone Traits in the Distal Femoral Epiphysis [Master's thesis]. Mount Sinai School of Medicine; 2008.
2008	Courtland H-W. Intra-Species Variation in Skeletal Mechanical Function is Achieved Through Genetic Regulation of Both the Quality and Morphology of Bone [PhD thesis]. Mount Sinai School of Medicine; 2008.
2008	Price C. Systems Based Approaches to Identifying How Genetically Varying Skeletal Growth Affects Skeletal Functionality and Fragility [PhD thesis]. Mount Sinai School of Medicine; 2008.
2012	Jimenez Palomar I. Mechanical Properties of Bone At the Sub-lamellar Level [PhD thesis]. London, England: Queen Mary University of London; September 2012.
2012	Emerson NJ. Development of Patient-Specific CT-FE Modelling of Bone Through Validation Using Porcine Femora [PhD thesis]. University of Sheffield; September 2012.
2012	Kwaczala AT. Alendronate and PTH Differentially Modulate Bone Quality and Reduce Adiposity in an OVX Rat Model [PhD thesis]. Stony Brook, NY: Stony Brook University; December 2012.
2002	Wohl GR. Bone Mechanics in Transplanted Osteochondral Grafts [PhD thesis]. Calgary, AB: University of Calgary; September 2002.
2004	LaMothe JM. Functional Adaptation of Bone [PhD thesis]. Calgary, AB: University of Calgary; September 2004.
2011	Barth HD. A Hierarchical Approach to Characterizing the Fracture Behavior of Bone Utilizing Synchrotron Radiation [PhD thesis]. Berkeley, CA: Berkeley, University of California; F 2011.
2010	Kulin RM. On the Dynamic Behavior of Mineralized Tissues [PhD thesis]. San Diego (UCSD), University of California; 2010.
2019	Mazur C. Osteocyte Regulation of Bone Quality in Homeostasis and in Skeletal Disease [PhD thesis]. San Francisco, University of California; 2019.
2022	Schurman CA. The Role of TGFβ Mediated Osteocytic Perilacunar/canalicular Remodeling in Age-Related Bone Fragility [PhD thesis]. San Francisco, University of California; 2022.
2023	Fuller LH. Structure-Function Relationships of Bighorn Sheep Horncore Bone and Horn-Horncore Interface Materials for Energy Absorption Applications [PhD thesis]. University of Massachusetts at Amherst; February 2023.
1994	Jepsen KJ. Characterization of the Hierarchical Composite Properties of Cortical Bone: A Transgenic Approach [PhD thesis]. University of Michigan; 1994.
1995	Tseng K-F. Investigating the Structure-Function Relationships of Long Bone: An Approach Using Growth Hormone Mouse Models [PhD thesis]. University of Michigan; 1995.
1998	Vajda EG. Age-Related Changes in the Microstructure and Mineralization of the Female Proximal Femur [PhD thesis]. University of Utah; March 1998.
2007	Rosenbaum TG. Effects of a Femoral Component and Patient Factors on Periprosthetic Cortical Bone [PhD thesis]. University of Utah; May 2007.
2012	Maloul A. Biomechanical Characterization of Complex Thin Bone Structures in the Human Craniofacial Skeleton [PhD thesis]. University of Toronto; 2012.
1998	Yeni YN. Fracture Mechanics of Human Cortical Bone: The Relationship of Geometry, Microstructure and Composition With the Fracture of the Tibia, Femoral Shaft and the Femoral Neck [PhD thesis]. Morgantown, WV: West Virginia University; 1998.
1993	Sedman AJ. Mechanical Failure and Antler: The Accumulation of Bone of Damage [PhD thesis]. York, UK: University of York; September 1993.